Evolution of The Size and Functional Areas of The Human Brain (Schoenemann 2006)

ANRV287-AN35-20 ARI 9 September 2006 8:42
Evolution of the Size

and Functional Areas
of the Human Brain
Annu. Rev. Anthropol. 2006.35:379-406. Downloaded from arjournals.annualreviews.org
by UNIVERSITY OF PENNSYLVANIA LIBRARY on 09/21/06. For personal use only.
P. Thomas Schoenemann
Department of Behavioral Sciences, University of Michigan–Dearborn,
Dearborn, Michigan 48128; email: ptoms@umich.edu
Annu. Rev. Anthropol. 2006. 35:379–406 Key Words

First published online as a Review in neuroanatomy, encephalization, behavior, adaptation, selection
Advance on June 16, 2006
The Annual Review of Anthropology is online Abstract

at anthro.annualreviews.org
The human brain is one of the most intricate, complicated, and
This article’s doi: impressive organs ever to have evolved. Understanding its evolu-
10.1146/annurev.anthro.35.081705.123210
tion requires integrating knowledge from a variety of disciplines in
Copyright c 2006 by Annual Reviews. the natural and social sciences. Four areas of research are particu-
All rights reserved
larly important to this endeavor. First, we need to understand basic
0084-6570/06/1021-0379$20.00 principles of brain evolution that appear to operate across broad
classes of organisms. Second, we need to understand the ways in
which human brains differ from the brains of our closest living rela-
tives. Third, clues from the fossil record may allow us to outline the
manner in which these differences evolved. Finally, studies of brain
structure/function relationships are critical for us to make behav-
ioral sense of the evolutionary changes that occurred. This review
highlights important questions and work in each of these areas.
379
INTRODUCTION specializations, and possible gene-expression

changes.1
The evolution of the human brain has been
Encephalization one of the most significant events in the
quotient (EQ): evolution of life. Although the outline of
calculated as the how and why this happened is being filled
ratio of a species’
PATTERNS OF BRAIN
in, many fundamental questions remain to EVOLUTION
actual brain size to
the size expected be answered. The fossil record, in concert
given its body weight with a comparative neuroanatomical analy- Brain/Body Scaling
sis of closely related species, shows that the How should species be compared with respect
hominid brain increased in size more than to brain size? It has long been known that
threefold over a period of approximately 2.5 brain size scales with body size across broad
million years. However, it has become in- groups of animals (Dubois 1913). For this rea-
creasingly clear that the human brain is not son, some measure of relative brain size has
simply a large ape brain: Important quali- usually been favored in comparative studies.
tative and quantitative changes occurred as Empirically the relationship between brain
well. Some of these changes are a result of and body size can be estimated using a func-
broad patterns of brain evolution that appear tion of the form [brain] = c[body]a , where c
across species, either for developmental rea- and a are empirically derived constants. Be-
sons or because of patterns of adaptation that cause the brain/body relationship is nonlin-
are inherent in the nature of life. Some are ear, a simple ratio of brain to body is prob-
presumably a result of direct selection for lematic (e.g., small animals have larger ratios
specific behavioral abilities of various kinds. than larger animals on average). Encephaliza-
Unraveling which adaptational explanations tion quotients (EQs) are widely used measures
are possible or likely requires understanding of relative brain size that take this empiri-
as much as we can about how brain struc- cal relationship between brain and body size
ture relates to behavioral variation. Unrav- into account. They are simply the ratio of a
eling the story of human evolution requires species’ actual brain size to the brain size ex-
research in each of these areas: (a) general pected for an animal of its body size ( Jerison
patterns of brain evolution, (b) compara- 1973). The expected brain size for a given
tive assessment of brain anatomy across species is usually derived using a regression
species, (c) the fossil history of human-brain (or other method, e.g., reduced major axis) of
evolution, and (d ) brain structure/function log brain to log body size for the compari-
relationships. son group of species, resulting in a formula of
This review focuses on trying to under- the type [log brain] = log c + a[log body].
stand evolutionary changes in brain size as Jerison (1973) used mammals as the compar-
well as the proportions of different brain ison group, but one can estimate EQs, for
areas. It highlights conceptual areas and example, on the basis of primates only. One
questions that are prone to misunderstand- can also extend the concept to subcomponents
ing, need particularly careful assessment, are of the brain and scale them either against
of current controversy, or present impor-
tant avenues for future research. It neces-
sarily leaves out some research areas that
1
are both important and interesting, such as I encourage those interested in extended reviews of human
brain evolution to consult Allman 1999, Deacon 1997, Falk
deep cortical and brainstem nuclei, the evo- 1992, Geary 2005, Holloway et al. 2004a, and Striedter
lution of specific neuron types and their 2005.
380 Schoenemann
body size or brain size (see, e.g., Schoenemann tunately, EQs are not so easily interpreted.
1997). If EQ really tells us something about intelli-
Because EQs are calculated on the basis gence or general behavioral complexity, what
Pongids:
of empirical estimates of brain/body-scaling are we to make of the large whales, who have larger-bodied apes,
relationships, they are sensitive to the partic- the lowest EQs of all mammals [e.g., hump- part of the taxonomic
ular sample used to derive a and c parame- back whales (Megaptera nodosa) have EQs superfamily
ters. Jerison (1973) originally estimated the of 0.18 (Schoenemann 1997)]? Humpback Hominoidea, which
include common and
scaling parameter a (i.e., slope) for mammals whales display a variety of complex behaviors,
bonobo
as ∼0.67, but Martin (1981) estimated it to including structured vocal sequences (songs?) chimpanzees,
be 0.76 using a larger sample. Using Jerison’s that last 5–25 min before repeating, and com- gorillas, and
(1973) equation, human EQs are ∼7, whereas plex feeding techniques, including the use of orangutans
Martin’s (1981) equation gives the values at bubble clouds to encircle prey (Rendell et al.
∼5. Regardless of the slope estimate used, 2001).
however, humans consistently have the high- Other species comparisons further high-
est values among mammals. light the problem: Guinea pigs (Cavia cut-
Figure 1 shows brain/body-size relation- ler) have significantly higher EQs (0.95) than
ships for a sample of 52 primate species and do elephants (Loxodonta africana, 0.63). This
illustrates different scaling estimates for sep- is true even though guinea pig brains weigh
arate primate subtaxa. Primates as a group only ∼3.3 g, whereas elephant brains can
tend to have larger brains than the av- weigh over 5700 g (Schoenemann 1997). If
erage mammal, with EQs for anthropoids EQ really tells us something important about
(all primates excluding prosimians) averag- behavior, this should be evident in a com-
ing ∼2 (i.e., anthropoids have brains ap- parison of guinea pig versus elephant be-
proximately twice the size of the average havior, yet this does not appear to be the
mammal of their body size). Even though case. If anything, given the variety of com-
absolute brain size is significantly larger plex social behaviors known in elephants (e.g.,
in pongids (chimpanzee, bonobo, gorilla, McComb et al. 2001), absolute brain size
orangutan) than in all other anthropoids ex- appears more behaviorally relevant in this
cept humans, they do not have substantially comparison.
larger EQs, indicating their brains are scal- In fact, a number of studies suggest that—
ing approximately similar to other anthro- for some behavioral domains—absolute brain
poids. Human brain sizes, by contrast, are size is more relevant than EQ. This is true for
not explained by brain/body scaling in either measures of the ease of learning abstract rules
mammals or primates. as opposed to simple associations (Rumbaugh
Although EQs are superficially appeal- et al. 1996), as well as the speed of learning
ing as a measure of comparative brain size, object-discrimination tasks (Riddell & Corl
it is unclear exactly how to interpret EQ 1977). In addition, although relative brain size
differences between species. The behavioral is often emphasized in brain/behavior studies,
relevance of EQ has long been questioned associations are invariably also significant if
(Holloway 1966), yet it is often incorrectly absolute brain volumes are used (e.g., Dunbar
assumed that it must be the most behav- 1995, Reader & Laland 2002). Jerison (1973)
iorally relevant variable of brain size—as if recognized this when he suggested an alter-
it were some coarse estimate of intelligence native to EQ: an estimate of extra neurons,
or other behavioral ability (e.g., Kappelman which is the absolute amount of neural tis-
1996). Others have uncritically assumed that sue beyond that predicted empirically by body
increases in absolute brain size may not be mass (e.g., two species with identical EQs but
meaningful if EQs remain the same (e.g., different body masses also differ in number
Wood & Collard 1999, Wynn 2002). Unfor- of extra neurons). This measure is, however,
www.annualreviews.org • Evolution of the Human Brain 381

not commonly used in discussions of hominid Under this model, body size varies ac-
brain evolution. cording to a variety of ecological constraints
The incorrect assumption that absolute and tends to put upper limits on possible
brain size is not particularly behaviorally rel- brain size, which in turn tend toward the
evant may stem from the fact that, because high end, particularly in social species (see be-
brain size scales with body size, it is assumed low). The human condition is explained by be-
growth of the two must be tightly constrained havioral adaptations that lead to a relaxation
together developmentally (e.g., Finlay et al. of ecological constraints. This behavioral-
2001). Such developmental constraints would selection/body-size-limiting model of brain-
require that a larger-bodied species have a size evolution is more consistent with the wide
larger brain, so simply comparing species in range of brain sizes at a given body size in
absolute brain size would improperly con- mammals, and it also explicitly does not as-
flate brain size with body-size differences. sume that EQ is the only behaviorally relevant
The problem with this view is that brain/body comparative measure. In addition, this model
scaling does not, in fact, necessarily imply de- is consistent with the finding that two genetic
velopmental constraint. Although the corre- loci known to be important to brain size de-
lation between brain and body size is high velopment, ASPM and microcephalin, both
(typically r > 0.95), at least a tenfold range show signatures of strong selection specifi-
of variation in absolute brain size exists at cally at the evolutionary divergence of the line
a given body size in mammals (Finlay et al. leading to pongids and hominids (away from
2001, Schoenemann 1997). Thus, any devel- all other primates) even though pongids do
opmental constraint would not appear to be not show an increase in relative brain size over
strong. In addition, it is not often recognized other primates (as noted above) (see Evans
that brain/body scaling could be the result et al. 2004, Wang & Su 2004).
of body size constraining brain size, rather In summary, brain size does scale with body
than the brain and body being tightly develop- size, and EQ differences do suggest something
mentally linked. Jerison’s (1973) explanation about the relative importance brains have had
for the brain/body relationship is that larger during a species’ evolutionary history, but they
bodies need larger brains both to control should not be used uncritically as proxies of
greater muscle mass and to process greater species’ behavioral capacities. That brain size
amounts of sensory information. Other ex- scales with body size across mammals does not
planations emphasize the limiting role of constitute strong evidence of developmental
metabolic resources in brain growth across constraints tying the two together. Absolute
species (Armstrong 1983, Martin 1981). In brain size itself appears to be behaviorally
either case, absolutely larger brains might relevant.
always be adaptive if they can be paid for
metabolically (and hence ecologically). Be- Patterns of Internal Brain Allometry
cause brains are metabolically expensive [i.e., Larger brains have more neurons (Haug
having high metabolic rates per gram of tissue 1987), but for these neurons to remain equally
(Aiello & Wheeler 1995, Hofman 1983b)], well connected to each other (in the sense
brain sizes tend to vary at a given body size of a signal having the same average num-
as a function of the usefulness of brains for a ber of synapses to traverse to travel between
particular species niche. Larger animals gen- any two neurons), the number of connections
erally have larger brains because they have (axons) must increase much faster than the
more metabolic resources available to put to- number of neurons (Ringo 1991). Hofman’s
ward brain development and maintenance, (1985) data show that white matter increases
not because of developmental constraints faster than gray matter with increasing brain
(Schoenemann 2004). size. (White matter contains longer-distance
382 Schoenemann
axonal connections between cortical areas, Because humans differ from other species
whereas gray matter contains most neuronal on a number of interesting behavioral dimen-
cell bodies and dendritic connections.) How- sions (e.g., communication, ability to harness
ever, the increase is not fast enough to main- technology, problem solving, complexity of
tain equal degrees of connectivity between social relationships; see below), and because
neurons (Ringo 1991). As brain size increases, the neural processing underlying these is
therefore, there is a concomitant increase in often located in different brain regions,
the separation between existing areas, lead- there is no general agreement about what
ing to a strong correlation between brain components are most important to study a
volume and the number of distinguishable priori. For this reason, this review covers
cortical areas across mammals (Changizi & most of the components for which infor-
Shimojo 2005). These scaling relationships mation is available. These include overall
predict ∼150 distinct cortical areas in hu- brain size, olfactory bulb, cerebellum, visual
mans. Although the human cortex is not yet cortex, temporal lobe, and the overall frontal
completely mapped, this predicted number is cortex and its components (primary motor,
broadly consistent with what is thought to be premotor, and prefrontal cortices). Because
the actual number (Van Essen et al. 1998). of space limitations, noncortical areas other
than the cerebellum (e.g., deep cortical and
brainstem nuclei) are not discussed here.
HUMAN BRAINS IN Behavioral implications of anatomical differ-
COMPARATIVE PERSPECTIVE ences are reviewed in the subsequent sections.
Understanding human brain evolution re- Our knowledge of anatomical differences is
quires the assessment of exactly how human further advanced than our knowledge of what
brains differ with respect to the size of various these differences might mean behaviorally. In
components from those of other living ani- general, however, it is generally assumed, im-
mals, particularly our closest evolutionary rel- plicitly or explicitly, that more tissue translates
atives: the pongids. Empirically mapping all into greater sophistication in neural process-
the possible differences across many species is ing in some way, which in turn suggests in-
an extraordinarily time-consuming task, and creased complexity of the behaviors mediated
at present we are nowhere near a complete by that particular area (or areas). Actual direct
understanding of all the differences that may tests of this assumption are relatively rare,
exist. Below I review the brain components however.
that have been studied in enough detail to
give at least preliminary assessments about
the relative status of human brains. The neu- Brain Size
roanatomical variables studied to date are ei- The most obvious evolutionary change dur-
ther relatively easy to measure or have been ing human evolution, as noted above, has been
thought to be particularly interesting behav- an increase in both absolute and relative brain
iorally. Because conscious awareness is local- size (Holloway 1995). Estimated brain sizes of
ized to areas of the cortex (the outermost our closest living relatives, the pongids (large-
layer of gray matter of the cerebral hemi- bodied apes), are as follows: common chim-
spheres), much comparative research has fo- panzee (Pan troglodytes), 337 (±16) cc; pygmy
cused on cortical subdivisions. In some ar- chimpanzee (P. paniscus), 311 (±11) cc; gorilla
eas, only the size of an entire cortical lobe (Gorilla gorilla), 397 (±67) cc; and orangutan
has been estimated in enough species to allow (Pongo pygmaeus), 407 (±29) cc (Rilling &
any comparison; in other areas, studies exist of Insel 1999). Modern human brain sizes vary
more-localized (and presumably functionally widely, but average ∼1330 cc (Dekaban 1978,
specific) areas. Garby et al. 1993, Ho et al. 1980a, Pakkenberg

& Voigt 1964).2 Modern human brains are Visual cortex. The visual cortex is so named
3.1 times larger than predicted on the basis because it is the site of the initial conscious
of primate brain/body-size allometric scaling processing of visual information. It is located
(Schoenemann 1997). in the occipital lobe, which is the most poste-
rior portion of the cortex. The human pri-
Olfactory bulb. The olfactory bulb is the mary visual cortex (the initial cortical area
first major processing area for the sense of devoted to processing visual information) is
smell. Stephan et al.’s (1981) data show that only ∼60% the size it should be for a pri-
the olfactory bulb is only ∼30% as large mate brain that size (Holloway 1992), but it
as predicted for primate brains of our size is ∼1.5 times larger in absolute terms than
(Schoenemann 1997). Because overall brain it is in chimpanzees (Stephan et al. 1981).
size is approximately three times larger in The human primary visual cortex is 5% larger
than expected given a primate of our body size
modern humans, this suggests the olfactory

bulb has lagged behind overall brain-size evo- (Deacon 1997, Schoenemann 1997). It is not
lution. This finding is consistent with the clear whether this says anything about relative
belief that olfaction is relatively poor in hu- visual processing abilities in humans. How-
mans, comparatively. However, the human ol- ever, given that the human primary visual cor-
factory bulb is ∼1.6 times larger than expected tex is smaller in relative terms, but larger in
for a primate of our body size (Schoenemann absolute terms, it could be used to test which
1997). Exactly how one should interpret dif- is more behaviorally relevant: If humans have
ferences relative to body size versus differ- behavioral advantages over apes in the visual
ences relative to brain size is a major unre- domain (specifically in those known to be me-
solved issue. It would appear that olfaction is diated by the primary visual cortex), it would
not unimportant. suggest that absolute amounts of neural tis-
sue would be more important than relative
Cerebellum. The cerebellum plays a key amounts, at least for visual processing. Such a
role in modulating patterns of muscle move- study has not been done.
ments and appears to play a role in timing Preuss & Coleman (2002) have docu-
generally. It may be involved in aspects of mented a variety of changes of the neurons in
language processing as well (Gazzaniga et al. the primary visual cortex in humans, partic-
1998). The human cerebellum is ∼2.9 times as ularly a population of interneuronal connec-
large as expected for a primate of our body size tions in layer 4a that appears to have expanded
(calculated from data in Stephan et al. 1981) significantly in human evolution. The exact
and as such has increased only slightly more behavioral significance is not known, but these
slowly than the brain as a whole. MacLeod changes emphasize that human-brain evolu-
et al. (2003) have shown that there is a grade tion involved more than simple changes in size
shift in hominoids with respect to the size of (relative or absolute) of brain regions.
the cerebellar hemispheres, with hominoids
as a group (humans included) showing greatly Temporal lobe. The temporal lobe plays a
enlarged cerebella compared with monkeys. critical role in auditory information, as well as
The cerebellum’s participation in language memory (through the hippocampal formation
presumably explains why it has not lagged be- and associated areas), emotion (amygdala),
hind as has the olfactory bulb, for example. and conceptual understanding (Carpenter &
Sutin 1983). As a result, it also plays an im-
portant role in language processing. Rilling &
2
Seligman (2002) report that humans have sig-
Original data in grams was converted to estimated cc using
the formula (brain volume in cc) = (brain mass in grams)/ nificantly larger overall volumes, white matter
1.036. European-derived samples only. volumes, and surface areas of their temporal
384 Schoenemann
lobes than predicted on the basis of ape scal- significantly more white matter volume in ar-
ing relationships. This suggests an elaboration eas close to the cortical surface than homi-
in humans of the behaviors mediated in this noid (pongids plus the smaller-bodied apes
lobe. such as gibbons and siamangs) data predict.
Calculating from their data (Schenker et al.
Frontal lobe. The frontal lobe consists of all 2005), human frontal cortical gray matter is
cortical areas anterior to the central sulcus 3.6 times larger than the average for their
(which angles inferoanteriorly to superopos- pongid sample, but human frontal gyral white
teriorly along the midlateral convexity of the matter is 4.7 times larger. This suggests a bias
cortex on both hemispheres).3 It contains a toward white matter expansion in humans, al-
number of different functional areas, includ- though the extent to which this is explained
ing the primary motor area (also known as statistically by allometric-frontal/nonfrontal
Brodmann’s area 4 to neuroanatomists, lo- (or some other) scaling cannot be deter-
cated immediately anterior and adjacent to the mined (e.g., total brain sizes are not re-
central sulcus), which directly controls con- ported). Because allometric explanations have
scious muscle movements; the premotor area neither straightforward behavioral implica-
(known as Brodmann’s area 6, located imme- tions nor developmental-constraint implica-
diately anterior to the primary motor area), tions, as discussed above, it is not clear what
which plans complex muscle-movement se- an allometric explanation would mean in any
quences; and the prefrontal cortex (everything case. However, it may reflect increased func-
anterior to the premotor area), which me- tional distinctions of areas within the frontal
diates a number of higher cortical functions lobe. In any case, the frontal lobe is, at a min-
important for planning, language, and social imum, more than three times larger than it is
interactions, as well as having a general exec- in pongids, and this likely has important be-
utive oversight of other brain regions (see behavioral implications of some kind. To under-
low). A number of studies have quantified the stand what these might be, it is useful to look
entire frontal cortex (which is relatively easy at specific subdivisions of the frontal lobe.
to delineate across species), without subdivid-
ing it into its functional subdivisions. Overall, Primary motor and premotor areas. Al-
the frontal lobe in humans appears to be as though the sample sizes are small (N = 7), the
large as expected, given a primate brain of our primary motor area in humans appears to be
size (Bush & Allman 2004, Semendeferi et al. only ∼33% as large as predicted for a primate
2002, von Bonin 1963). Semendeferi et al. brain our size (Blinkov & Glezer 1968). This
(2002) report that human frontal cortex aver- suggests our primary motor cortex has scaled
aged 37.7 (±0.9)% of the entire brain, com- approximately with absolute body size during
pared with 35.4 (±1.9)% for common chim- human evolution (Deacon 1997). Given that
panzees, 34.7 (±0.6)% for bonobo, 36.0% for this area mediates the direct conscious control
gorilla, and 37.6 (±1.1)% for orangutan. of muscle movements, and given that humans
However, recent data suggest a difference do not seem particularly gifted or particularly
with respect to gray matter/white matter pro- poor comparatively with respect to muscle
portions of the frontal lobe, which suggest po- control, this approximate scaling with body
tentially important behavioral implications. size (but not brain size) argues against the im-
Schenker et al. (2005) report that humans have portance of relative amounts of neural tissue
for behavioral ability, at least for this area.
The human premotor area, just anterior to
3
The surface of the cortex is not smooth but is folded back the primary motor area, also appears smaller
and forth upon itself, resulting in patterns of indentations
referred to as sulci (singular, sulcus) separated by ridges than predicted given absolute brain size, al-
referred to as gyri (singular, gyrus). though not to the same extent. The premotor

area is ∼60% as large as predicted for a not follow obvious sulcal/gyral gross morpho-
primate brain our size (Blinkov & Glezer logical features, it is not possible to exactly
1968).4 This suggests the premotor area has delineate it using structural MRI. However,
not lagged as far behind as the primary motor a proxy for prefrontal cortex volume can be
area as brain size increased. Taken together, used: cortical volume anterior to the corpus
these two findings suggest an elaboration of callosum (the major tract of white matter con-
motor planning but not an increase in motor necting the two hemispheres). This proxy is
control per se. No direct tests of these sug- commonly applied to both human (e.g., Raz
gestions have been reported, however. et al. 2005, Sax et al. 1999) and nonhuman pri-
mate (Lyons et al. 2002; variant in McBride
Prefrontal. If the entire frontal lobe is ap- et al. 1999) studies. Estimated in this way, hu-
proximately as large as expected given over- man prefrontal cortex was shown to be signif-
icantly larger than in pongids (Schoenemann
all human brain size, yet the two portions

of the frontal lobe reviewed above (the pri- et al. 2005b). Specifically, human values av-
mary motor and premotor areas) are signif- eraged 12.7% of total brain volume, com-
icantly smaller, then the rest of the frontal pared with an average of 10.3% for the four
lobe (i.e., the prefrontal) must necessarily be pongid species. Nonprefrontal cerebral vol-
larger than expected (Preuss 2000). There ume in humans averaged 3.7 times larger than
is nevertheless currently some controversy the average of P. paniscus and P. troglodytes,
over this point. Brodmann’s original cytoar- but the prefrontal portion averaged 4.9 times
chitectural studies, which form the basis for larger.
much of our knowledge of cortical areas, Assessing both Semendeferi et al.’s (2002)
strongly point to significantly larger pre- data on the total frontal lobe and our own
frontal cortices in humans compared with data, it appears that if the analysis is restricted
other primates (Brodmann 1909). Allomet- to increasingly anterior regions of the frontal
rically, Brodmann’s data suggest the human (keeping in mind that the prefrontal occu-
prefrontal is ∼2 times larger than predicted pies the most-anterior portions of the frontal
on the basis of the size of the rest of the lobe), humans appear increasingly dispropor-
brain (Deacon 1997). The suggestion of bi- tionate. With respect to allometric scaling,
ased expansion is also supported by research total human frontal cortex is slightly smaller
quantifying the degree of folding in different than predicted (Semendeferi et al. 2002), but
parts of the cortex: Humans appear to have the prefrontal (using our proxy) is slightly
substantially more convoluted (and hence, a larger than predicted (Schoenemann et al.
greater volume of) cortex in prefrontal re- 2005b). Given that the prefrontal proxy used
gions (Armstrong et al. 1991, Rilling & Insel appears to underestimate human values much
1999). more so than other primates (Schoenemann
Studies using magnetic resonance imag- et al. 2005a), this strongly suggests that human
ing (MRI) to quantify prefrontal cortex also prefrontal is in fact larger, both as a percentage
support this contention. Because the poste- of total brain volume, as well as allometrically.
rior boundary of the prefrontal cortex does Our data do not allow a clear confirmation of
whether human prefrontal cortex is actually
twice the predicted size, however.
4
Semendeferi et al. (2002) report that human precentral In addition, the human difference ap-
gyrus volumes (expressed as percent of total cortex; i.e.,
not allometrically) fall within the range of their hominoid peared biased toward white matter rather
sample. However, because the precentral gyrus does not than gray matter (Schoenemann et al. 2005b).
contain all of the motor cortex, and only contains a small Comparing humans with chimpanzees, pre-
portion of the premotor cortex, it is not clear exactly what
this suggests about either motor or premotor cortex size in frontal gray volumes averaged 4.8 times
humans. larger in humans, whereas nonprefrontal gray
386 Schoenemann
volumes averaged 4.2 times larger. By con- Within the prefrontal itself, studies sug-
trast, prefrontal white volumes averaged 5.0 gest a mosaic of evolutionary changes. A cy-
times larger in humans, whereas nonpre- toarchitectural study of Brodmann’s area 13,
frontal white volumes averaged only 3.3 a subdivision of the prefrontal that medi-
times larger. Furthermore, the human average ates aspects of social behavior (particularly
value was significantly allometrically larger emotional dimensions), suggests that this area
as well, although not to the extent found in lagged behind the expansion of the brain as a
Brodmann’s original data. Sherwood et al. whole: It is only 1.5 times larger than the av-
(2005) point out that prefrontal white volume erage pongid value (Semendeferi et al. 1998).
is predicted by prefrontal gray volume in our By contrast, another subdivision of the pre-
dataset, suggesting that the difference appears frontal, Brodmann’s area 10, which is known
to be in proportions of prefrontal versus non- to mediate tasks involving planning and or-
prefrontal. Given that a critically important ganization of thought and future behavior
role of the prefrontal is to moderate activity (Carpenter & Sutin 1983), is 6.6 times larger
in posterior cortical areas, this apparent shift in humans than in pongids (Semendeferi et al.
in proportions likely has important behavioral 2001). Holloway (2002) notes this is actu-
implications, as discussed below. ally only slightly more than one would pre-
Additional support for the biased expan- dict given how area 10 scales with brain size.
sion of the prefrontal comes from work mor- This is because the relationship is strongly
phing primate brains into human brains. positively allometric (i.e., as brain size in-
Deformation maps describing the necessary creases, area 10 seems to increase much
transformations allow for detailed, global faster).
assessments of morphological differences. How should we interpret these findings
Comparisons between humans and bonobo in subareas of the prefrontal? First, as dis-
(P. paniscus) (Zilles 2005), common chim- cussed above, even if allometry statistically
panzees (P. troglodytes) (Avants et al. 2005), predicts some increase in humans, this does
and macaque monkeys (Van Essen 2005) have not license us to conclude that the increase
been reported. In all three cases, substantial is behaviorally irrelevant (Schoenemann et al.
increases in the prefrontal region were re- 2005a). Nor does the existence of allometric
ported. Our own group found that the av- scaling constitute a demonstration of the exis-
erage common chimp–human difference was tence of inherent developmental constraints.
approximately twofold for some prefrontal ar- Larger brains may have larger prefrontal cor-
eas (Avants et al. 2005). To date, these stud- tices (or subregions therein) because selec-
ies involve comparisons between only two tion places greater demands on the oversight
species, so scaling trends across primates can- role of prefrontal areas as posterior regions
not be estimated. However, it should be possi- become more complex. As discussed above,
ble to extend these analyses to multiple species absolute amounts of cortical tissue have been
comparisons, resulting in separate allometric- shown to be correlated with a variety of be-
scaling estimates—and extent of human di- havioral dimensions. Thus, even though area
vergence, if any—for individual areas at high 13 is relatively smaller than one would pre-
resolution. Furthermore, the morphing algo- dict, it might nevertheless indicate an im-
rithms can be applied to collections of cell- portant behavioral change, particularly given
stained brain sections, thereby combining the the enhanced interactive sociality that has in-
resolution of detailed cytoarchitectural analy- creasingly characterized the human condition
ses (studies of patterns of neurons in the cor- (see below). Increases in area 10 almost surely
tex) with the ability of morphing algorithms suggest increased importance in the various
to quantify changes in shape. dimensions of behavioral planning.

FOSSIL EVIDENCE OF HUMAN the likelihood of punctuational events. Re-

BRAIN EVOLUTION cent empirical analyses of cranial capacity
What is known about the evolutionary his- changes over time support this notion (De
tory of these apparent differences in brain Miguel & Henneberg 2001, Lee & Wolpoff
anatomy? The goal of research in this area 2003). Furthermore, it is not clear how im-
is to determine exactly what can be inferred portant species designations (which are inher-
about the behavior of fossil hominids from ently problematic for fossils) are for under-
imprints on the inside surface of their brain- standing brain-size evolution. De Miguel &
cases. This is of central importance to un- Henneberg (2001) showed that 90% of the
derstanding human brain evolution. Because variation in fossil hominid brain size can be
of this intrinsic interest in the behavior of explained simply by the age of fossils, leaving
fossil hominids, a great deal of effort has only 10% to be explained by species differ-
ences and/or measurement error. This sug-
been spent trying to extract maximal inference

out of minimal data. Because brains do not gests that most of the brain size increase dur-
fossilize, the richness of comparative data is ing hominid evolution was not closely tied to
always greater than the fossil data. The fol- speciation events.
lowing subsections highlight these limitations
and serve to illustrate the inherent difficulty of Lunate Sulcus
the task. At present, the fossil record is clear-
est for overall brain size as indexed by cranial The portion of the cortex that has received
capacity, although other suggestive clues have perhaps the greatest amount of attention in
been found regarding possible early changes fossil specimens is the visual cortex. A sul-
in different brain regions related to visual pro- cus known as the lunate marks the anterior
cessing and language. boundary of the primary visual cortex in non-
human primates, although it is often miss-
ing in humans (Allen et al. 2005a, Connolly
1950). In relative terms, an anterior position
Cranial Capacity of the lunate (and therefore anterior extent of
Cranial capacity is by far the most well- the primary visual cortex) is characteristic of
attested change in human brain evolution the general pongid condition, whereas a pos-
in the fossil record. Figure 2 plots cranial terior placement is characteristic of modern
capacity estimates against estimated speci- humans. As discussed above, the primary vi-
men age for published hominid fossils dat- sual cortex is a relatively smaller portion of
ing from 15 KYA to 4 MYA, a total the human brain in comparison with chim-
of 145 individual specimens. It is apparent panzee brains, even though in absolute terms
from Figure 2 that changes in hominid brain it is ∼1.5 times larger than that of either chim-
size began sometime between 3 and 2 Mya. panzees or gorillas (Stephan et al. 1981).
Although it has been argued that brain The evolutionary history of this change has
size has undergone punctuational (i.e., not been the source of considerable controversy
continuous and gradual) change at vari- over the years: Did it occur early in hominid
ous points during hominid evolution (e.g., evolution (e.g., in early Australopithecines),
Hofman 1983a), Figure 2 suggests the range thereby signaling some form of early reappor-
of variation at any particular point in time tionment (Holloway prefers the term reorga-
(best exemplified in modern species) com- nization) of neural resources? Or was it simply
bined with the sparse sampling evident for the result of the primary visual cortex lagging
particular time periods of our evolutionary behind as brain size increased during human
history (e.g., between 1.0 and 0.5 Mya) in- evolution? Holloway and Falk have, over the
dicate that it may be premature to assess years, disagreed on the possible positioning of
388 Schoenemann
the lunate sulcus on brain endocasts attributed social behavior including communication.”
to both Australopithecus africanus (Taung) and Thus cortical expansion anterior to the lunate
A. afarensis (AL 162–28, 3.2 Mya) (e.g., Falk is argued to have behavioral implications, but
1987, Holloway 1995). Holloway believes the reduction posterior to the lunate is argued to
lunate either cannot be seen (Taung) or is be behaviorally meaningless. If the size of the
likely in a modern human posterior position primary visual cortex really is irrelevant, why
(AL 162–28) in early Australopithecines, long do humans have 1.5 times as much primary
before substantial changes in absolute brain visual cortex, given the evolutionary costs of
size occurred. Falk and others have argued brain tissue (see below)? If Holloway and col-
that it likely occurred later, as a result of brain leagues are right about the location of the lu-
size increases in other cortical regions. De- nate in AL 162–28 and STW 505 (which they
bates over the position of the lunate have seem to be), it is either behaviorally meaning-
not been resolved, in part because it is dif- less, or Australopithecines had reduced visual
ficult to assess its location unequivocally on processing capabilities of some kind. Both
endocast specimens and because of disagree- these alternatives are problematic. Thus, at
ments about the proper orientation of the AL this point it is not clear how to interpret the
162–28 specimen. Holloway and colleagues position of the lunate in fossil specimens.
(Holloway et al. 2004b) have recently re-
ported on another A. africanus specimen,
STW 505, which they show appears to have a Broca’s Area
relatively posterior lunate. Evidence relevant to the origin of language is
In addition, Holloway et al. (2003) dis- intrinsically of great interest. There is some
cuss the brains of two apparently normal suggestion of the elaboration of Broca’s area
chimpanzees that nevertheless have lunates (a key cortical region that plays a central role
in human-like posterior locations. They note in language processing, located in the left pre-
this finding demonstrates the possibility of a frontal portion of the inferior frontal lobe) in
posterior lunate in the absence of increased fossil hominids. Holloway (1983) noted that a
brain size, which means Holloway’s long-held Broca’s cap (an endocranial bump over what
contention of a posterior shift in early small- would be Broca’s area) is present—although
brained hominids is certainly possible. How- inconsistently—in pongids. Thus, the pres-
ever, these specimens also complicate behav- ence of a Broca’s cap does not definitively indi-
ioral interpretations of the apparent change. cate the existence of language, unfortunately.
Holloway et al. (2003) argue that the reduc- Tobias (1975) and Holloway (1983) argue
tion of the primary visual cortex has no behav- that Broca’s cap becomes increasingly present
ioral implications. However, if a chimpanzee in early Homo, however (see also Broadfield
can have a human lunate pattern (presumably et al. 2001). Tobias (1983) argues this indicates
indicating a reduced primary visual cortex), early Homo had language. Both Falk (1983)
this pattern is not a clear indicator of human- and Holloway (1995) agree that the endocast
like behavior, and therefore the location of of the early Homo specimen KNM-ER 1470
the lunate in fossil endocasts may not be be- (1.8 Mya) looks more modern-human-like in
haviorally interpretable, rendering the lunate the inferior frontal region. Although this does
sulcus debate moot. not prove that KNM-ER 1470 had a Broca’s
However, Holloway and colleagues area or that it had language, it nevertheless
(Holloway et al. 2004b, p. 6) argue that a suggests something important is occurring in
posterior lunate in Australopithecines “indi- this region. Broadfield et al. (2001) report that
cates an expanded posterior parietal cerebral the specimen Sambungmacan 3 has asymmet-
cortex [anterior to the primary visual cortex], rical Broca’s caps, which they speculate may
and was most likely associated with enhanced indicate a level of language ability beyond

that found in earlier hominids. This spec- However, because the hominid pattern
imen is assumed to be Middle Pleistocene occurs in a fair number of pongid specimens,
Homo erectus, although it is unfortunately the functional significance of this finding is
Petalias: areas
where the brain not well provenienced (Marquez et al. 2001). obviously not clear. It cannot be considered
extends farther in Thus, suggestive (but equivocal) evidence ex- definitive evidence of any particular behavior
some direction for ists of possible language-related changes in in individual specimens.
one hemisphere over the brains of early Homo, dating back to
another
almost 2 Mya.
Summary of the Fossil Evidence
It is clear that brain evolution started in
Asymmetry earnest sometime between 2 and 3 Mya. Al-
Because important aspects of behavior are though punctuated models of brain size in-
asymmetrically organized (e.g., key compo- crease can be fit to the data, there is no com-
nents of language are usually processed in pelling reason to assume anything other than
the left hemisphere, which is usually also the a reasonably constant trend toward increas-
dominant hemisphere for hand movements), ing brain size over time. Apart from cranial
it is of interest to determine whether cortical capacity, only suggestive, equivocal clues of
asymmetries can be found that predict these possible behavioral patterns are evident in
behavioral asymmetries, thereby possibly the fossil record of hominid brain evolution,
allowing us to infer behavior from fossil speci- mostly relating to the question of language
mens. Research to date has centered on partic- evolution. Although definitive statements are
ular anatomical asymmetries known as petal- not currently warranted, we do not presently
ias. Holloway & de la Coste-Lareymondie know the limits of possible inferences about
(1982) report that only modern and fossil ho- the behavior of fossil hominids from their en-
minids (including australopithecines, H. erec- docranial remains. The intrinsic interest in
tus, and Neanderthals) show a consistent, reconstructing hominid behavior ensures that
distinct right-frontal and left-occipital petal- every possible avenue of inference will be ex-
ial pattern. Pongids also show petalias, but plored in the future. It is certainly possible that
they did not display the same degree of con- additional associations between cranial form
sistency, particularly in the combination of and brain anatomy (and ultimately behavior)
right-frontal and left-occipital petalias. Only will eventually be uncovered using modern
25% of pongids assessed displayed this pat- morphometric methods.
tern, compared with 82% of hominids. Falk
et al. (1990) demonstrated that Rhesus mon-
keys (Macaca mulatta) show a significant ten- EVOLUTION OF BRAIN AND
dency toward right-frontal petalias (although BEHAVIOR
not to the same consistency as found in mod- Explaining the anatomical changes in the hu-
ern and fossil hominids) but not for left- man brain reviewed in the sections above re-
occipital petalias. Thus it appears that petal- mains a central question in human evolu-
ias in general are common in anthropoids, tionary studies. Exactly why these changes
but the particular pattern of petalias and happened, and what they might mean behav-
the degree of consistency appear unique to iorally, is a question of fundamental impor-
hominids. tance. As with any evolutionary change, there
Holloway & de la Coste-Lareymondie are two basic kinds of explanation: adaptive
(1982) speculate this right-frontal/left- change (the result of selection) and nonadap-
occipital petalial pattern may be related to tive change (the result of genetic drift). Adap-
right-handedness, language-related symbol tive explanations are probably the strongest
manipulation, and spatio-visual integration. for questions of brain evolution as compared
390 Schoenemann
with almost any other biological characteris- tion. If so, there would have been some an-
tic. This is partly because of the pattern of cestral populations in which individuals with
changes and partly because of the apparent larger-than-average brain sizes did not have
evolutionary costs involved in the changes, reproductive advantages. [This might explain
both of which strongly argue for adaptive the possible decrease in brain size from Ne-
explanations. anderthal to modern humans (Schoenemann
Although genetic drift can lead to the 2004).] However, on average over our evolu-
fixation of particular alleles at a single lo- tionary history, reproductive benefits needed
cus by chance, the odds that an evolution- to have been at least marginally greater for
ary succession of alleles at a variety of loci larger-brained individuals.
(e.g., see Gilbert et al. 2005) leads progres-
sively in a particular direction (e.g., larger
brain size) is extraordinarily unlikely. In ad- Brain Evolution Through Behavioral
dition, these changes have occurred in the Selection

face of apparently strong evolutionary costs As the various mental faculties gradually
(Smith 1990). Costs in this context refer to developed themselves the brain would almost
correlated effects that—everything else be- certainly become larger. No one, I presume,
ing equal—ultimately translate into decreased doubts that the large proportion which the size of
numbers of offspring produced per unit time. man’s brain bears to his body, compared to the
These costs have to be paid every generation. same proportion in the gorilla or orang, is closely
First, as noted above, the brain is among the connected with his higher mental powers.
most metabolically expensive organs in the Darwin 1871, p. 145
body [i.e., neural tissue has among the highest Given that larger brain sizes must have
metabolic rates per gram (Aiello & Wheeler provided individuals with reproductive ad-
1995, Hofman 1983b)]. Second, increasing vantages during significant portions of our
brain size in primates is strongly correlated evolutionary history, it is reasonable to ask
with longer gestation periods, an increased both (a) what exactly the advantages were,
period of infant dependency, and delayed re- and (b) whether these advantages still exist
production (Harvey & Clutton-Brock 1985), within modern humans (and/or other living
which all decrease the number of offspring an primates). Although Gould (1981) suggested
individual can produce per unit time. Third, that variation in brain size is behaviorally
there is an apparent trade-off in bipedal ho- meaningless in modern populations, it is not
minids between locomotor efficiency and ease at all clear why we should expect brain size
of childbirth (Lovejoy 1975). Fourth, there above some threshold to have absolutely no
is potentially a problem of cooling a larger advantage. The simplest a priori model would
brain (Falk 1990). If there were no counterbal- posit a behavioral benefit (or usefulness), on
ancing advantages to larger amounts of brain average, to larger brains that would be present
tissue, individuals with smaller brains would regardless of whether the particular benefit
necessarily have a selective advantage. translated into reproductive advantages in any
For adaptive evolutionary change to oc- given environment. The behavioral benefit
cur, reproductive benefits must have con- might be, for example, greater memory ability,
sistently (or at least on average) accrued planning ability, or linguistic ability. Whether
to individuals—within successive popula- such benefits were evolutionarily meaning-
tions connecting ancestral and descendent ful depends on the degree to which they
populations—who varied anatomically from helped pay (reproductively) for the evolution-
the average of their populations. Of course, ary costs associated with larger brains. This,
brain size may not have uniformly and grad- in turn, depends on the specific ecological
ually increased in every successive popula- and social conditions characteristic of a given

population. An increasingly powerful linguis- we posit a small genetic correlation of only

tic processor is likely not worth the costs for a r = 0.05 and heritabilities (i.e., the propor-
species that is not highly socially interactive, tion of phenotypic variation in a population
Genetic
correlation: occurs for example. More complex models regard- explained by genetic variation) of 0.3, the se-
when changes in the ing costs and benefits of increasing brain size lected individuals (i.e., those who contribute
genetic effects on are of course possible (e.g., wildly nonlinear to the subsequent generation) only have to
one trait have the relationships between behavioral abilities and differ from their overall population average
effect of changing
brain size). However, parsimony requires in- by less than 0.006 standard deviations on the
the other trait
vestigating simpler explanations first. hypothesized directly selected characteristic
Heritability: the
For selection on some behavioral abil- (Schoenemann et al. 2000). This is so small
proportion of
phenotypic ity to cause evolutionary changes in brain that it would be extremely difficult to demon-
(observable) variance anatomy, there must necessarily have been strate empirically. Although the strength of
of a characteristic in a genetic correlation between them. Failing selection could have varied over time dur-
a population that is this, selection on behavior would have no evo- ing our evolutionary history, these estimates
explained by genetic
lutionary effect on brain anatomy, and we clearly demonstrate that we do not need to
variance in that
population would lack an explanation for evolutionary hypothesize more than a weak genetic corre-
changes in the brain. Attempts to assess such lation to explain the dramatic change in brain
brain/behavior correlations are therefore cen- size via selection on correlated behavioral
tral for any model that posits the evolution- characteristics.
ary importance of behavior in human brain This does not mean, however, that the
evolution. genetic correlation must therefore be small
It is also not generally appreciated, how- and that there is no justification for assessing
ever, that the genetic correlation between be- genetic correlations within humans without
havior and brain size does not actually have to massive sample sizes. It simply shows that it
be large to explain human brain-size evolution need not be large. Because of the evolutionary
(Schoenemann et al. 2000). This is partly be- costs described above, it is highly unlikely that
cause the rate of change in brain size per gen- the correlation was in fact zero (or negative),
eration is only ∼8 mm3 (assuming a 1000-cc as that would require some unknown non-
increase in brain size over 2.5 million years behavioral explanation for increasing brain
and a 20-year average generation length) (see size.
Figure 2), or approximately 0.0002 standard
deviations of chimpanzee-brain size (see also
Holloway et al. 2004a). The size of the ge- Evidence of Genetic Correlations
netic correlation needed to account for this Between Brain and Behavior
amount of change per generation is partly a There is substantial evidence that many fea-
function of the strength of selection operat- tures of brain anatomy are influenced by ge-
ing on the hypothesized correlated (directly netic factors. In a number of studies, re-
selected) variable (e.g., some behavioral abil- searchers have reported heritability of brain
ity), as well as of the extent to which both brain size to be significant, with estimates rang-
size and the selected variable are genetically ing from 0.66 to 0.94 (reviewed in Winterer
influenced, or heritable (Falconer 1981).5 If & Goldman 2003). Heritability estimates of
the patterns of sulci and gyri on the cortical
surface are generally significantly lower, al-
5
The strength of selection and the size of the genetic corre- though this may be an artifact of the difficulty
lation interact to determine the likely amount of change per of quantifying them (Winterer & Goldman
generation. Assuming reasonable heritabilities, the same 2003). Thompson et al. (2001) estimated in-
amount of change can occur if either selection is strong
and the genetic correlation is weak, or if selection is weak dependent heritabilities for each voxel (the
but the genetic correlation is strong. smallest unit of volume in an MRI image) of
392 Schoenemann
cortical gray matter in a sample of monozy- third variable affecting both the brain and be-
gotic and dizygotic twins and found evidence havior (or other hypothesized evolutionarily
for widespread genetic influence. Volumes relevant correlate) in similar directions. So-
of the left and right frontal lobes have esti- cioeconomic status, for example, is correlated
mated heritabilities of between 0.52 and 0.66 with both IQ scores (Herrnstein & Murray
(Geschwind et al. 2002), and a number of 1994) and growth of the body (Bogin 1999),
Brodmann areas (including some prefrontal and one might therefore predict a spurious
regions) appear to have at least moderate correlation between brain size and IQ on this
heritabilities (Wright et al. 2002). Thus, basis. In addition, cross-assortative mating
brain anatomy appears to be under genetic can result in phenotypic correlations between
influence. characteristics that actually have completely
Similarly, cognitive abilities have been independent genetic influences ( Jensen &
shown to have genetic influence. Although in- Sinha 1990). If the correlation between brain
telligence is a controversial concept in some size and some behavior is spurious, selection
areas of the social sciences, the consensus on that behavior cannot explain evolutionary
among those who research individual dif- changes in brain size. It is therefore critically
ferences in cognitive ability is that genetic important to assess the strength of the genetic
influences on general cognitive ability (g)6 correlation, not just the phenotypic correla-
are substantial, although environmental influ- tion, between the brain and behavior.
ences are also clearly evident (Neisser et al. One way to control for possible con-
1996). Genetic influences have also been founds is by assessing the strength of the
demonstrated for other cognitive domains, association between brain size and behav-
such as verbal and spatial factors, although the ior among siblings within families. Family
degree to which these genetic factors are inde- members share essentially the same socio-
pendent of g is not always clear (Plomin et al. economic status (this can be directly assessed),
1997). and meiosis ensures siblings contain random
Although there is evidence of genetic in- associations of alleles at different loci, thereby
fluences on both brain and behavior, to what eliminating cross-assortative mating effects.
extent are these influences genetically cor- To date, only a few studies have used this
related? A large number of studies reported methodology. Two within-family studies us-
finding phenotypic (not genetic) correlations ing head circumference as a proxy for brain
between brain size and behavioral ability (usu- size have reported equivocal results ( Jensen
ally g, or other IQ-related abilities). Obvi- 1994, Jensen & Johnson 1994; see discus-
ously, our ancestors were not selected to do sion in Schoenemann et al. 2000). Only a few
well on modern IQ tests, but some of the MRI studies have been reported to date. Our
abilities tapped by these tests possibly were own group found essentially no correlation
selected for. Studies using MRI to estimate (r = −0.05, NS) within families between
actual brain size report correlations averaging brain size and an estimate of g in 36 pairs of
r = ∼0.45 (Rushton & Ankney 1996). adult sisters (Schoenemann et al. 2000). An-
However, these are phenotypic correla- other study of male-sibling pairs reported a
tions, not genetic correlations, and are there- nonsignificant but positive within-family cor-
fore not necessarily evolutionarily relevant. relation of r = 0.23 between brain size and
Phenotypic correlations could be caused by a g (Gignac et al. 2003). In addition, a recent
study using a genetically informative cohort
of 24 monozygotic pairs, 31 dizygotic pairs,
6
Performance on a wide variety of cognitive tests is corre- and 25 additional nontwin siblings estimated
lated. g is a measure that statistically explains these corre-
lations and as such is typically interpreted as a measure of a genetic correlation between g and both gray
general cognitive ability. IQ tests are good measures of g. and white matter volumes of r = 0.29 and

r = 0.24, respectively (both p < 0.05) that are conceivably evolutionarily relevant
(Posthuma et al. 2002). The genetic correla- have also been found, including spatial ability,
tion for overall brain size was not reported, working memory, and the ability to extract
unfortunately, but was presumably similar relevant information from a distracting
(given that gray + white = total brain). environment.
One unresolved issue is the direction of Spatial ability has been the focus of re-
causality. It has long been known that envi- search partly because it was proposed to help
ronmental influences can affect brain volume, explain sex differences in brain size, which av-
specifically cortical gray matter volume in rats erage ∼1 standard deviation (Ho et al. 1980b).
(Diamond 1988). This means that genes with Some but not all of this difference is explained
higher g could be causing individuals to ex- by body weight (Ankney 1992, Falk et al.
perience more-stimulating and complex en- 1999) and/or fat-free weight (Schoenemann
vironmental situations, which may in turn 2004). Because males and females differ on
cause developmental (not genetic) increases average in spatial ability, in Western popula-
in their brain sizes and cortical gray volumes tions at least (Halpern 1987), if spatial ability
(Posthuma et al. 2003). If this were the sole correlates strongly with brain size, the resid-
reason for the brain size/g correlation, then ual sex difference in brain size might therefore
selection for g is not likely the explanation for be explained. However, many studies, includ-
our increased brain sizes during our evolu- ing the more recent genetically informative
tionary history because it implies brain-size MRI-based ones, have failed to find a signifi-
variation is solely a developmental response. cant association between brain size and spatial
However, some of the brain size/g correlation abilities (Posthuma et al. 2003, Schoenemann
is likely explained through g influencing brain et al. 2000, Wickett et al. 2000).
size, which means that the evolutionarily crit- Spatial-ability differences still may ex-
ical association—in which brain size causes plain differences in the shape of the cor-
(or allows for) changes in g—is likely smaller pus callosum, which in women appears to be
than the r = 0.24 to r = 0.29 genetic corre- larger in the posterior region (e.g., Davatzikos
lations suggested by Posthuma et al.’s (2002) & Resnick 1998, de Lacoste-Utamsing &
study. Holloway 1982). This portion of the corpus
Taken together, these studies suggest the callosum, known as the splenium, connects
genetic correlation between brain size and g areas of the parietal lobes known to medi-
is not zero but is not as large as the phenotypic ate spatial tasks. Thus, Holloway and col-
correlations typically reported for MRI stud- leagues (Holloway et al. 1993) have suggested
ies of brain volume and g mentioned above. the anatomical difference in corpus callosum
The proportion of genetic variance in g ex- morphology may therefore be explained by
plained by genetic variance in brain volume sex differences in spatial abilities. Consistent
appears substantially less than 8.5%. This is with this suggestion, our own group has re-
still large enough to explain the evolution of cently found that women with smaller (more
brain size in hominids, however. male-like) splenia score better on a test of
mental rotation–spatial ability (P.T. Schoene-
Other behavioral measures. Although mann, A. Dubb, J. Hu, J. Lewis & J. Gee, un-
most research has focused on correlations published manuscript).
with behaviors associated with general cogni- Working-memory abilities (i.e., the abil-
tive ability, natural selection may have acted ity to manipulate information in short-term
on other unrelated behavioral dimensions as memory to solve particular problems or goals)
well as (or instead of ) general cognitive abil- appear to be associated with dimensions of
ity. Associations between neuroanatomical brain size (r = 0.40, p < 0.05 for gray mat-
variation and other behavioral dimensions ter; r = 0.33, p < 0.05 for white matter)
394 Schoenemann
(Posthuma et al. 2003). Because the prefrontal (remember) what actions or behaviors lead
cortex is known to be particularly important to to exactly which outcomes. Thus serial-order
the mediation of working memory (Goldman- memory likely played a key role in human be-
Rakic 1996), Posthuma et al.’s finding is of havioral evolution. Although no studies have
particular interest in light of the possible bi- addressed whether serial-order memory is as-
ased increase in the prefrontal cortex during sociated with prefrontal size (or size of some
human evolution discussed above. Working other region), this would seem to be a fruitful
memory abilities have been shown to corre- direction to pursue.
late with the length of the main prefrontal sul-
cus (principal sulcus) across a variety of Old
and New World monkeys, and this correla- Brain Size and Conceptual
tion completely explains the association be- Complexity
tween working-memory ability and cranial ca- A general argument can be made that increas-
pacity across these species (Redmond 1999). ing brain size brought with it an increase in
This raises the question of whether the as- conceptual or semantic complexity (Gibson
sociation found by Posthuma et al. (2003) in 2002). Jerison (1985, p. 30) suggested that
humans is actually more properly localized “[g]rades of encephalization presumably cor-
to the prefrontal cortex (which unfortu- respond to grades of complexity of informa-
nately was not separately delineated in their tion processing. These, in turn, correspond in
study). some way to the complexity of the reality cre-
The size of the prefrontal cortex in hu- ated by the brain, which may be another way
mans has been shown to correlate with the to describe intelligence.”
Stroop task within families (Schoenemann A number of observations support this
et al. 2000). This test measures the extent of view. First, concepts are instantiated in the
linguistic interference in naming colors, when brain as webs or networks of activation be-
ink color and word name are mismatched tween different areas (see Pulvermuller 2001).
(e.g., the word red written in blue ink). It is Most of our subjectively experienced concepts
generally considered a test of the ability to ex- are actually complex combinations of sensory
tract (and focus on) the relevant information information processed in various ways by the
from an environment and is known to be me- different cortical centers. Taste, for example,
diated by prefrontal areas. is actually a complex interaction of olfactory
The prefrontal cortex also mediates a va- (smell) and gustatory (taste) inputs (e.g., the
riety of additional particularly interesting be- flavor of a banana is largely olfactory). Sim-
haviors, including planning (Damasio 1985), ilarly, the auditory perception of a phoneme
memory for serial order and temporal in- can be altered if it is paired with a mismatched
formation (Fuster 1985), aspects of language visual input (McGurk & MacDonald 1976).
(Deacon 1997), and social information pro- This means there must be networks connect-
cessing (de Bruin 1990). The importance of ing differing regions as well as areas that me-
serial-order memory is generally not appreci- diate the integration of this information.
ated in discussions of human behavioral evo- To what extent is brain size relevant to con-
lution. One of the clearest behavioral advan- ceptual complexity? Larger-brained species
tages humans have over other organisms is have more complicated networks of intercon-
the ability to reconstruct, understand, and uti- nection, thereby leading to greater potential
lize causal information. All human technolog- conceptual complexity (Lieberman 2002). It
ical sophistication is dependent on this ability. has long been known that certain areas of the
In turn, causality is dependent on the ability body (e.g., the lips and hands) are dispro-
to remember the serial order of past events. portionately represented in the somatosen-
Without this, it is impossible to reconstruct sory and primary motor areas of the brain

and that these match differences in the degree for language of Broca’s and Wernicke’s ar-
of sensitivity and/or motor control for differ- eas has been known for more than a cen-
ent parts of our body (Penfield & Rasmussen tury, but it has become increasingly clear
1950). Thus, even within species, we have that language requires the cooperation of a
a clear association between the amount of wide range of cortical areas, including the
cortical tissue and behavioral dimensions cerebellum (Gazzaniga et al. 1998), right-
(Gibson 2002). Animals with specific behav- hemisphere areas [important for process-
ioral specializations (e.g., bat echolocation) ing logical inferences encoded in language
have correlated increases in areas of the brain (Beeman et al. 2000)], prefrontal cortex [im-
known to mediate those behaviors (Krubitzer portant for higher-level language function-
1995). ing (Novoa & Ardila 1987)], and areas of the
We can then add to this the tendency for frontal lobe outside Broca’s area (Alexander
larger-brained animals to display greater de- et al. 1989). Functional brain imaging stud-
grees of cortical specialization: Individual ar- ies suggest the prefrontal cortex also plays a
eas tend to be more specific in function and critical role in conceptual/semantic process-
less directly connected to other areas. This ing (Gabrieli et al. 1998). All of this indicates
is critical to conceptual complexity because that language draws on a wide array of neural
it increases the brain’s potential to differen- resources, which suggests that important fea-
tiate complex sensory information into di- tures of brain evolution may be explained by
verse constituent parts, thereby helping to the coevolution of language (Deacon 1997).
magnify subtle differences between different That language evolution is specifically rel-
streams of sensory input. The argument can evant to brain-size evolution has been sug-
be summarized as follows: Increasing brain gested many times (e.g., Dunbar 1996, Gibson
size leads to increasingly complex process- 2002, Wang 1991, Washburn 1960). Darwin
ing within areas, greater degrees of auton- (1871, p. 57) himself argued that, although
omy between areas, and greater complexity language use during human evolution likely
of the possible interactions between areas. had effects on the elaboration of the vocal
This leads to a greater complexity of possible organs, “the relation between the continued
network-activation states, which is equivalent use of language and the development of the
to a greater degree of conceptual subtlety and brain has no doubt been far more important.”
sophistication possible in the organism’s rep- Brain size, in this view, is itself an index of lan-
resentations of reality. Whatever else increas- guage evolution. This suggests language has
ing brain size led to in hominid evolution, it is origins that are substantially older than the
difficult to escape the conclusion that concep- appearance of anatomically modern H. sapi-
tual complexity increased substantially during ens, which date to perhaps ∼160,000 years
this time. Furthermore, given the fundamen- ago (White et al. 2003). As reviewed above,
tally socially interactive nature of humans, as the trend toward increasing brain size began
well as the general association between degree sometime before 2 Mya (Figure 2). Although
of sociality and brain size (discussed below), there is widespread disagreement about how
this increase in conceptual complexity is likely far back language extends in human evolution
directly relevant to the evolution of language. (for a review, see Schoenemann 2005), it is dif-
ficult to escape the conclusion that language
likely played a major role in the evolution of
Brain Evolution and Language the human brain. The evidence of the rela-
Although the exact evolutionary changes in tionship between brain size and conceptual
the brain necessary to allow for language are complexity at a minimum suggests that funda-
not known, language clearly relies on a large mental changes in human cognition critical to
number of neural resources. The importance language evolution began prior to ∼2 Mya.
396 Schoenemann
Sociality and Brain Evolution Dunbar (1996) has further argued that
human language represents a form of social
Primates in general, and humans in particu-
grooming that allowed the increase in group
lar, are socially interactive animals. Our ability
size beyond that otherwise possible. Although
to survive and reproduce is at least as depen-
there are a number of extrapolations needed
dent on successfully navigating social arrange-
to arrive at this conclusion, language clearly
ments as it is navigating the physical envi-
serves a highly social function in humans.
ronment (Holloway 1975, Humphrey 1984).
Although the comparative evidence that
Social interactions are intrinsically compli-
social complexity correlates with brain size is
cated, and the complexity increases with in-
strong, the specific abilities crucial to social
creasing social group size. Humphrey (1984)
ability within humans (or any other species)
pointed out that the increasing complex-
are not clearly defined or understood. Some
ity of the social world selects for increasing
people are more social than others, and some
cognitive sophistication (social intelligence)

social people are better at understanding
in individuals, which in turn creates even
and/or manipulating social interactions than
more complex social interactions. This creates
others. However, there does not appear to
a cycle of ever-increasing social complexity,
have been much research into this question
leading to ever-increasing intellect among
from a neurocognitive and/or neuroanatomi-
individuals—what Humphrey refers to as
cal standpoint. Presumably social competence
an evolutionary ratchet. Because of the
depends on a wide variety of abilities, in-
apparent benefits of being skilled at so-
cluding language, nonverbal-cue processing,
cial manipulation in such an increasingly
memory (particularly of past interactions and
complex social existence, this has become
the order of past events), and probably many
known as the Machiavellian intelligence
other basic cognitive abilities. Interestingly,
hypothesis.
intact prefrontal cortex (unlike other corti-
It appears likely that selection for social
cal areas) appears to be crucial for the main-
abilities was an important influence on brain
tenance of high position in dominance hier-
evolution. A number of comparative studies
archies in monkeys (de Bruin 1990, Myers
of primates have confirmed an association be-
et al. 1973). Given that this area seems to have
tween measures of brain and/or neocortex
undergone disproportionate increase, as dis-
size (both absolute and relative) and a vari-
cussed above, this appears to be a promising
ety of measures of social complexity, includ-
avenue of investigation with respect to brain
ing mean social group size, social clique size,
evolution. Other parts of the brain that ap-
frequency of reported acts of deceptive be-
pear to be important for social behavior in-
havior, amount of social play (but not nonso-
clude the amygdaloid nuclei and overlying
cial types of play), and the degree to which
temporal pole (tip of the temporal lobe) and
male-dominance rank fails to accurately pre-
the posterior medial orbital cortex (including
dict mating success (see review in Dunbar
Brodmann’s area 13, located in the inferior
2003, and references therein). All of this is
prefrontal cortex) (Kling 1986). As reviewed
consistent with the idea that brain size is a fac-
above, Brodmann’s area 13 shows a moder-
tor in social ability, broadly defined, although
ate increase in absolute terms, although it
there are glaring exceptions: Orangutans are
does lag behind the increase of the brain as
relatively large-brained but relatively aso-
a whole. Piecing together the effects the so-
cial. Clearly, brain size is not a perfect func-
cial environment had on modifying the brain
tion of social complexity. However, there
during human evolution will likely continue
is no other known behavioral variable that
to be the focus of significant research in the
correlates as highly with brain size across
future.
species.

Ecological Hypotheses volume. Although early hominid stone-tool

industries are not highly complex technolog-
An alternative (but not mutually exclusive)
ically, they may have required cognitive abil-
hypothesis is that adaptation for ecological
ities beyond that shown by apes, for example,
challenges influences brain evolution. Milton
in the sequencing of required actions (Toth &
(1981) pointed out that different types of diet
Schick 1993). A preliminary functional brain–
vary with respect to the cognitive demands
imaging study of stone-tool manufacturing
they place on individuals. Fruit is patchily
suggests the activation of cortical areas me-
distributed in both time and space, whereas
diating spatial cognition, as well as motor, so-
leaves are much less cognitively demanding
matosensory, and cerebellar areas (as might
to obtain. This suggests that species that
be expected given the nature of the task), al-
specialize in fruit (or, more generally, any food
though prefrontal areas known to be rele-
source that is cognitively demanding to ob-
vant to planning were not significantly acti-
tain) are expected to have larger brains than

vated (Stout et al. 2000). If this finding can
species that do not. Dunbar (1995) did not find
be replicated, given that spatial ability does
a significant association between a measure of
not appear significantly correlated with brain
relative brain size (ratio of the neocortex to the
size in modern humans (as discussed above),
rest of the brain) and percent of fruit in diet in
it may argue against early stone-tool manu-
anthropoid primates. However, Barton (1996)
facturing specifically spurring brain-size evo-
did find a significant association within diur-
lution (although the spatial abilities tested
nal haplorhines (specifically, diurnal monkeys
involved paper-and-pencil tests, rather than
and apes) between absolute and relative brain
hands-on, three-dimensional manipulation as
size and percent of fruit in the diet. This dis-
in the stone-tool study). Research on the pos-
crepancy is possibly a result of a difference in
sible importance of stone-tool manufacturing
neuroanatomical variables used.
is clearly in its infancy, and future functional-
It is also possible that the causality runs
imaging studies are needed to clarify the
the other way: Because larger brains are more
issue.
metabolically expensive, some sort of dietary
It has also been suggested that the develop-
accommodation may be necessary to pay for it
ment of accurate throwing might have spurred
nutritionally. The expensive-tissue hypothesis
brain evolution. Calvin (1983) pointed out
(Aiello & Wheeler 1995) argues for a trade-
that human throwing accuracy requires tim-
off between brain and gut size. If larger brains
ing abilities (for the release of the thrown
mean smaller guts, then one would predict a
object) that far exceed the probable timing
higher quality diet. This hypothesis is sup-
accuracies of neurons (judging from measure-
ported in primates (Fish & Lockwood 2003).
ments of the intrinsic variability in neuronal
It also fits the human case, in which brain size
signals). He pointed out that increasingly ac-
started increasing at about the same time as
curate timers could be built by putting greater
meat became increasingly important in ho-
and greater numbers of even inaccurate neu-
minid diets (as indexed by the initial appear-
rons in parallel in a timing circuit. He also sug-
ance of stone tools).
gested that, given the cortical areas in the pri-
mary motor cortex controlling the mouth and
tongue (involved in language) and the hand
Tools and Brain Evolution (involved in throwing) were reasonably close
Is it possible that the cognitive demands of to each other, selection for throwing abil-
tool making itself spurred brain evolution? ity may have led to changes that preadapted
Reader & Laland (2002) showed that fre- the brain for language. This hypothesis has
quency of tool use in primates is positively cor- proven difficult to test, but it may be con-
related with both absolute and relative brain sistent with the tentative finding that the
398 Schoenemann
premotor cortex in humans may not have shown to be genetically influenced, genetic
lagged as far behind as the primary motor correlations between brain anatomy and be-
cortex during human brain evolution. It is havior appear to be quite modest. The genetic
also consistent with the finding that sequen- correlation between overall brain size and
tial finger tapping is disrupted by concurrent general cognitive ability appears to be sub-
speech (which depends on the left hemisphere stantially smaller than overall phenotypic cor-
in most individuals) only if the tapping is done relation. Associations between specific func-
with the right hand (which is also controlled tional areas and specific behavioral abilities
by the left hemisphere) and not the left hand appear to be somewhat more robust.
(which is controlled by the right hemisphere) A number of general behavioral models
(Ikeda 1987). of brain evolution have been proposed that
have theoretical and/or cross-species empir-
ical support. These include the idea that
The Cognitive Reserve Hypothesis brain size is associated with increased concep-
An additional explanation for the increase tual complexity, language ability, social abil-
in brain size in human evolution is that it ity, ecological challenges, the development of
may have allowed for an increase in longevity tools, and the need for a cognitive reserve.
(Allen et al. 2005b, Humphrey 1999). The ar- Direct tests of these hypotheses await future
gument is that larger brains would buffer in- research.
dividuals against a variety of inevitable brain
insults as individuals age, thereby increasing
the useful cognitive lifespan. The results of a CONCLUSION
variety of clinical studies are consistent with Over the past 2 to 3 million years, our brain
the idea that larger brain size has a protective has changed in dramatic and behaviorally in-
effect for a number of brain diseases and types teresting ways. Although brain size and body
of injury (reviewed in Allen et al. 2005b). Why size are correlated, absolute increases in neu-
(and whether) longevity would be evolution- ral tissue are likely behaviorally relevant, and
arily adaptive in humans is unclear, although the overemphasis on EQ needs to be tem-
the survival of older, postreproductive indi- pered. There is substantial evidence that the
viduals has been argued to be important (e.g., human brain is also not simply a larger version
the grandmother hypothesis). The cognitive of a generic primate brain, with some areas
reserve hypothesis and the idea that more neu- showing evidence of lagging behind (such as
ral resources translate into better cognitive the olfactory bulb, primary visual cortex, pri-
functioning of some kind are not mutually ex- mary motor and premotor areas) and some ac-
clusive, of course. counting for disproportionate increases (such
as the prefrontal). We should expect to find
clues about the details of the behavioral evo-
Summary of the Evolution of Brain lution of our species from these patterns.
and Behavior Given the evolutionary costs of neural tis-
Explaining why the human brain changed as sue, disproportional increases (even in abso-
it did requires determining the behavioral im- lute terms) would not likely have occurred
plications of changing brain size and/or the unless they conferred some sort of adaptive
proportions of various brain components. To (reproductive) advantages, on average, to in-
be evolutionarily relevant, associations be- dividuals in the successive populations. The
tween the brain and behavior must be genetic advantages could be slight, however, making
correlations. These correlations can be quite our task as scientists potentially difficult. Gen-
small, however. Although both brain mor- eral cognitive ability appears to show weak
phology and behavioral dimensions have been associations with brain size, and a number

of behavioral dimensions appear to be asso- tion, methods, and resources from a wide va-
ciated with specific brain areas. Hypotheses riety of fields will increasingly be marshaled
involving conceptual complexity, social abili- to the task of squeezing every last possible
ties, language, ecological challenges, tool use, bit of valid inference out of the data. Fun-
and the cognitive reserve hypothesis all ap- damentally, our arguments will always nec-
pear to have merit for explaining human brain essarily be statistical judgments. At present,
evolution we do not even know the limits of what we
Filling out the history of human brain evo- can and cannot know about this history. Dis-
lution will continue to utilize an intensively covering these limits is a central task for the
interdisciplinary approach in which informa- future.
ACKNOWLEDGMENTS
I wish to thank Vincent Sarich, John Allen, Ralph Holloway, Dean Falk, Tim White, Thomas
Budinger, Arthur Jensen, Bruce Lahn, Karen Schmidt, Janet Monge, Dan Glotzer, Michael
Sheehan, and Reina Wong for stimulating discussions on the topics discussed in this review.
Any errors that remain are my own, of course.
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406 Schoenemann
AN35-20-Schoene.qxd 9/9/06 10:02 AM Page C-1
10,000
1000
100
Brain mass (g)
10
Average mammal
Prosimii
1 Ceboidea
Cercopithecoidea
Hominoidea
Homo sapiens
0.1
0.01 0.1 1 10 100 1000
Body mass (kg)
Figure 1
Brain/body relationships among primates. (a) Individual species plotted with Martin’s (1981)
estimate for the average mammal. (b) Least squares–regression estimates for various primate subtaxa.
All primates (excluding humans): [log brain g] 1.24 0.761 [log body kg], r2 0.92, N 51;
Hominoidea (excluding humans): [log brain g] 1.548 0.553 [log body kg], r2 0.99,
N 6; Cercopithecoidea: [log brain g] 1.54 0.477 [log body kg], r2 0.87, N 14; Ceboidea:
[log brain g] 1.35 0.765 [log body kg], r2 0.94, N 13; Prosimii: [log brain g] 1.111 0.659
[log body kg], r2 0.92, N 18. Data extracted from literature sources (see Schoenemann 1997 for
details); pongid data estimated from cranial capacities using [brain weight g] [cranial capacity cc]/
1.14 (following Kappelman 1996).
www.annualreviews.org ● Evolution of the Human Brain C-1

10,000
1000
100
Brain mass (g)
10
Average mammal
All primates
Prosimii
Ceboidea
1
Cercopithecoidea
Hominoidea
Homo sapiens
0.1
0.01 0.1 1 10 100 1000
Body mass (kg)
Figure 1
(Continued)
C-2 Schoenemann
2000
A. afarensis H. habilis Pan troglodytes
A. aethiopicus H. ergaster Extant H. sapiens sapiens
1800
A. boisei H. rudolfensis
A. robustus H. georgicus
A. africanus H. erectus
1600
A. garhi H. antecessor
H. soloensis
1400
H. heidelbergensis
H. sapiens neanderthalensis
H. sapiens idaltu
Cranial capacity (cc)
1200 H. sapiens sapiens
1000
800
600
400
200
0
4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0
Ma
Figure 2
Cranial capacity in fossil hominids over time. Extant chimpanzees (Pan troglodytes) and humans
(Homo sapiens sapiens) are included for comparison. Fossil data and species designations from Holloway
et al. 2004a. Pan and Homo species data compiled from literature sources listed in Schoenemann (1997).
www.annualreviews.org ● Evolution of the Human Brain C-3

Contents ARI 13 August 2006 13:30
Annual Review of
Anthropology
Volume 35, 2006
Contents
Prefatory Chapter
On the Resilience of Anthropological Archaeology

Kent V. Flannery p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Archaeology
Archaeology of Overshoot and Collapse

Joseph A. Tainter p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p59
Archaeology and Texts: Subservience or Enlightenment
John Moreland p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 135
Alcohol: Anthropological/Archaeological Perspectives
Michael Dietler p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 229
Early Mainland Southeast Asian Landscapes in the First
Millennium a.d.
Miriam T. Stark p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 407
The Maya Codices
Gabrielle Vail p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 497
Biological Anthropology
What Cultural Primatology Can Tell Anthropologists about the

Evolution of Culture
Susan E. Perry p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 171
Diet in Early Homo: A Review of the Evidence and a New Model of
Adaptive Versatility
Peter S. Ungar, Frederick E. Grine, and Mark F. Teaford p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 209
Obesity in Biocultural Perspective
Stanley J. Ulijaszek and Hayley Lofink p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 337
ix
Evolution of the Size and Functional Areas of the Human Brain

P. Thomas Schoenemann p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 379
Linguistics and Communicative Practices
Mayan Historical Linguistics and Epigraphy: A New Synthesis

Søren Wichmann p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 279
Environmental Discourses
Peter Mühlhäusler and Adrian Peace p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 457
Old Wine, New Ethnographic Lexicography
Michael Silverstein p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 481
International Anthropology and Regional Studies
The Ethnography of Finland

Jukka Siikala p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 153
Sociocultural Anthropology
The Anthropology of Money

Bill Maurer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p15
Food and Globalization
Lynne Phillips p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p37
The Research Program of Historical Ecology
William Balée p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p75
Anthropology and International Law
Sally Engle Merry p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p99
Institutional Failure in Resource Management
James M. Acheson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 117
Indigenous People and Environmental Politics
Michael R. Dove p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 191
Parks and Peoples: The Social Impact of Protected Areas
Paige West, James Igoe, and Dan Brockington p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 251
Sovereignty Revisited
Thomas Blom Hansen and Finn Stepputat p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 295
Local Knowledge and Memory in Biodiversity Conservation
Virginia D. Nazarea p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 317
x Contents
Food and Memory

Jon D. Holtzman p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 361
Creolization and Its Discontents
Stephan Palmié p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 433
Persistent Hunger: Perspectives on Vulnerability, Famine, and Food
Security in Sub-Saharan Africa
Mamadou Baro and Tara F. Deubel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 521
Theme 1: Environmental Conservation

Archaeology of Overshoot and Collapse

Joseph A. Tainter p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p59
The Research Program of Historical Ecology
William Balée p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p75
Institutional Failure in Resource Management
James M. Acheson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 117
Indigenous People and Environmental Politics
Michael R. Dove p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 191
Parks and Peoples: The Social Impact of Protected Areas
Paige West, James Igoe, and Dan Brockington p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 251
Local Knowledge and Memory in Biodiversity Conservation
Virginia D. Nazarea p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 317
Environmental Discourses
Peter Mühlhäusler and Adrian Peace p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 457
Theme 2: Food
Food and Globalization

Lynne Phillips p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p37
Diet in Early Homo: A Review of the Evidence and a New Model of
Adaptive Versatility
Peter S. Ungar, Frederick E. Grine, and Mark F. Teaford p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 209
Alcohol: Anthropological/Archaeological Perspectives
Michael Dietler p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 229
Obesity in Biocultural Perspective
Stanley J. Ulijaszek and Hayley Lofink p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 337
Food and Memory
Jon D. Holtzman p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 361
Contents xi
Old Wine, New Ethnographic Lexicography

Michael Silverstein p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 481
Persistent Hunger: Perspectives on Vulnerability, Famine, and Food
Security in Sub-Saharan Africa
Mamadou Baro and Tara F. Deubel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 521
Indexes
Subject Index p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 539

Cumulative Index of Contributing Authors, Volumes 27–35 p p p p p p p p p p p p p p p p p p p p p p p p p p p 553
Cumulative Index of Chapter Titles, Volumes 27–35 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 556

Errata
An online log of corrections to Annual Review of Anthropology chapters (if any, 1997 to
the present) may be found at http://anthro.annualreviews.org/errata.shtml
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ANRV287-AN35-20 ARI 9 September 2006 8:42

Evolution of the Size

Annu. Rev. Anthropol. 2006. 35:379–406 Key Words

The Annual Review of Anthropology is online Abstract

INTRODUCTION specializations, and possible gene-expression

www.annualreviews.org • Evolution of the Human Brain 381

www.annualreviews.org • Evolution of the Human Brain 383

modern humans, this suggests the olfactory

www.annualreviews.org • Evolution of the Human Brain 385

all human brain size, yet the two portions

www.annualreviews.org • Evolution of the Human Brain 387

FOSSIL EVIDENCE OF HUMAN the likelihood of punctuational events. Re-

been spent trying to extract maximal inference

www.annualreviews.org • Evolution of the Human Brain 389

dition, these changes have occurred in the Selection

www.annualreviews.org • Evolution of the Human Brain 391

population. An increasingly powerful linguis- we posit a small genetic correlation of only

www.annualreviews.org • Evolution of the Human Brain 393

www.annualreviews.org • Evolution of the Human Brain 395

cognitive sophistication (social intelligence)

www.annualreviews.org • Evolution of the Human Brain 397

Ecological Hypotheses volume. Although early hominid stone-tool

tain) are expected to have larger brains than

www.annualreviews.org • Evolution of the Human Brain 399

www.annualreviews.org • Evolution of the Human Brain 401

Endocasts: The Paleoneurological Evidence. Hoboken, NJ: Wiley & Sons

www.annualreviews.org • Evolution of the Human Brain 403

strates of cognition in hominoids. J. Hum. Evol. 49:547–69

www.annualreviews.org • Evolution of the Human Brain 405

Washburn SL. 1960. Tools and evolution. Sci. Am. 203:63–75

Brain mass (g)

Body mass (kg)

www.annualreviews.org ● Evolution of the Human Brain C-1

Brain mass (g)

Body mass (kg)

1200 H. sapiens sapiens

www.annualreviews.org ● Evolution of the Human Brain C-3

Volume 35, 2006

On the Resilience of Anthropological Archaeology

Archaeology of Overshoot and Collapse

What Cultural Primatology Can Tell Anthropologists about the

Evolution of the Size and Functional Areas of the Human Brain

Linguistics and Communicative Practices

Mayan Historical Linguistics and Epigraphy: A New Synthesis

Michael Silverstein p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 481

International Anthropology and Regional Studies

The Ethnography of Finland

The Anthropology of Money

Food and Memory

Theme 1: Environmental Conservation

Archaeology of Overshoot and Collapse

Food and Globalization

Old Wine, New Ethnographic Lexicography

Subject Index p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 539

Cumulative Index of Chapter Titles, Volumes 27–35 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 556

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